Development of invasive pink salmon ( Oncorhynchus gorbuscha Walbaum) eggs in a large Barents Sea river

Abstract The spawning and egg development of invasive pink salmon Oncorhynchus gorbuscha were investigated in the large River Teno in the Barents Sea area where they spawned for the first time on a large scale in 2021. The spawning period started in early August and egg development was rapid. All eggs were eyed by mid‐September and the first juveniles hatched in late September. In early October most eggs had hatched. Degree‐days in water temperature suggested that egg deposition had mostly taken place in early August. Early egg development is discussed in relation to possible consequences for survival.

After their introduction to the Russian White Sea basin in the late 1950s (Alekseev et al., 2019), pink salmon (Oncorhynchus gorbuscha Walbaum) gradually established naturally spawning populations in the White and Barents Sea Rivers, in both Russia and Norway (Sandlund et al., 2019). The current pink salmon population in the north-east Atlantic area originates from a single introduction in 1985 from the Ola River, a North Okhotsk Sea drainage in the Magadan oblast, which has resulted in a self-reproducing odd-year population (Gordeeva et al., 2015) spanning over 18 successive generations until today.
The slow development turned into a rapid, widespread increase in the distribution and abundance of pink salmon in the North Atlantic area in 2017 (Sandlund et al. 2019;VKM et al., 2020). The high abundances persisted, especially in the Barents Sea area, in 2019 and even higher run sizes were detected in 2021 (VKM et al., 2020;Anon, 2021).
The life cycle of O. gorbuscha is widely studied in their native range in the Pacific area (e.g., Groot & Margolis, 1991;Quinn, 2018, and references therein), and many characteristics of the species' life history are well-documented in the new Atlantic distribution area (e.g., Gordeeva et al., 2015;Alekseev et al., 2019). As timing of reproduction is one of the most critical adaptations of animal populations to their environment, the ideal spawning time of fish species or populations should result in emergence of juveniles at a date that optimizes their survival (Quinn, 2018). Although there are published studies revealing the development of O. gorbuscha eggs in different thermal regimes, to hatching and further until emergence, most of these studies have been carried out in hatcheries or controlled experimental facilities and little if any information is available from natural river habitats (Groot & Margolis, 1991, Quinn, 2018. We observed spawning of O. gorbuscha in a large Barents Sea River, the subarctic River Teno (Tana in Norwegian) in the northern part of  (Figure 2). Spawning redds were excavated by hand and shovel, and eggs/alevins were collected to a dip net held next to the redd downstream that effectively collected the eggs and alevins exposed to drift. We aimed at sampling 20-30 eggs/alevins per sampling period, but the actual catch varied between 7 and 115 (mean 33, S.D. 22) depending on the size of the redds and the environmental conditions. In addition, dead eggs were counted ( Table 1).
Proportions of eggs and alevins were estimated using a Bayesian Dirichlet-multinomial model. We assumed that the observed number of eggs/alevins sampled at spawning redd i at site s during week t that belong to life stages 1, 2 or 3 (noneyed, eyed, alevin) (x i,1:3,s,t ) follow a multinomial distribution: Here, N i,s,t is the total number of eggs/alevins sampled from spawning redd i at site s during week t and p 1:3,s,t is the vector of probabilities that an individual sampled at site s during week t belongs to life stages 1, 2 or 3. Furthermore, an uninformative Dirichlet-prior distribution was given for parameter p 1:3,s,t as: Note that only individuals sampled at the same site during the same week share a common prior distribution, that is, the individuals in different site/week combinations are considered independent from each other. We chose this approach because of simplicity, but a hierarchical structure could have been used, for example across the sites in the same week. This would have likely pushed the estimated proportions closer to zero in cases where zero individuals of a certain category were observed at multiple sites (see Table 1).
Water temperature in the main stem of the Teno River ( In all three sampling areas some noneyed eggs (2%-37%, estimated mean proportions using a Bayesian Dirichlet-multinomial model; Figure 2) were still present in early September (week 36), whereas in mid-September (week 37), all remaining eggs were already eyed and some hatched juveniles were found in late September (week 39; Table 1 and Figure 1). In early October (week 40) a mix of eyed eggs (23%-45%) and hatched alevins (55%-75%) were detected in redds, and in late October almost only alevins were found (82%-97%). In November (week 45), river ice formation allowed access to only one spawning area and a mean of 93% of the individuals sampled was estimated to be alevins ( Figure 2).
The number of dead eggs observed was low: the mean numbers across sampling areas varied from 0-3 eggs in September to 0-5 in early October and no dead eggs were observed in late October or November (Table 1).
Water temperature in the Teno mainstem was about 8 C during the first sampling in early September, dropped to 5-6 C in late September, increased to 7-8 C in week 40 and then decreased sharply to 0.1 C and below for the rest of the sampling periods in late October and November (Figure 1).
The exact date of egg deposition and start of incubation for the sampled spawning redds was naturally unknown, so we used our own visual observations of spawning activity in the sampling areas to create three scenarios for possible egg fertilization times. The first active spawning was observed during 2-3 August, followed by very high numbers of spawning fish and redds present at spawning grounds between 13 and 15 August. Finally, few spawners, mostly females, were still active on 10 September. Thus, three cumulative degree-day curves were fitted starting on 1 August, 15 August and 10 September (Figure 1).

Earlier studies suggest that the degree-days ( C) needed from
O. gorbuscha egg fertilization to eyed stage is about 350-400 (Kraus, 1999) and to hatching varies between 530 and 650 (Bailey et al., 1980, Hebert et al., 1998Kraus, 1999). Linking the observed developmental stages of eggs and alevins (Figure 2) to the degreedays in the Teno River in the three spawning time scenarios (Figure 1), it appears that most spawning and egg fertilization must have fol- The early spawning of O. gorbuscha in the River Teno is in fairly good accordance with that observed in the Russian White Sea basin (Alekseev et al., 2019), where spawning commenced when the water temperature was between 8 C and 10 C. However, Alekseev et al.
(2019) reported that spawning starts in this area between 10 and 15 August, which appears to be slightly later than in the River Teno.

AUTHOR CONTRIBUTIONS
J.E. and P.O. conceptualized the study. H.P conducted the data analysis. All authors participated in fieldwork, sampling, and writing and editing the manuscript.

ACKNOWLEDGEMENTS
We are grateful for information on spawning sites and occurrence of spawning Oncorhynchus gorbuscha in the Teno River from several people, especially Pekka Tuuri, and for field assistance from Annelea Vuontela. Comments from two anonymous reviewers helped improve the manuscript.

ETHICS APPROVAL
Specimens used in this study were sampled during investigations conducted under permission from the Centre for Economic Development, Transport and the Environment of Lapland (LAPELY 567/5713-2018) to the Natural Resources Institute Finland (Luke).